Nutrition practice, compliance to guidelines and postnatal growth in moderately premature babies: the NUTRIQUAL French survey

HAL Id: hal-01477012

https://hal.univ-reunion.fr/hal-01477012

Submitted on 25 Jun 2018

HAL is a multi-disciplinary open access archive for the deposit and dissemination of sci- entific research documents, whether they are pub- lished or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

Distributed under a Creative Commons Attribution| 4.0 International License

Nutrition practice, compliance to guidelines and postnatal growth in moderately premature babies: the

NUTRIQUAL French survey

Silvia Iacobelli, Marianne Viaud, Alexandre Lapillonne, Pierre-Yves Robillard, Jean-Bernard Gouyon, Francesco Bonsante

To cite this version:

Silvia Iacobelli, Marianne Viaud, Alexandre Lapillonne, Pierre-Yves Robillard, Jean-Bernard Gouyon, et al.. Nutrition practice, compliance to guidelines and postnatal growth in moderately premature babies: the NUTRIQUAL French survey. BMC Pediatrics, BioMed Central, 2015, 15 (1), pp.110.

�10.1186/s12887-015-0426-4�. �hal-01477012�

R E S E A R C H A R T I C L E Open Access

Nutrition practice, compliance to guidelines

and postnatal growth in moderately premature babies: the NUTRIQUAL French survey

Silvia Iacobelli

, Marianne Viaud

, Alexandre Lapillonne

, Pierre-Yves Robillard

, Jean-Bernard Gouyon

, Francesco Bonsante

and for the NUTRIQUAL group

Abstract

Background: The nutritional care provided to moderately premature babies is poorly studied. For a large cohort of such babies, we aimed to describe: nutrition practice intentions, comparison of the intended with the actual practice, compliance of actual practice to current nutrition guidelines, and postnatal growth.

Methods: A questionnaire was sent out to 29 neonatal intensive care units in France, in order to address practice intentions. In the same units, retrospective patient ’ s data were collected to assess actual practice, compliance to nutrition guidelines and infant postnatal growth. The cumulative nutritional deficit during the two first weeks of life was calculated and variables associated with Δ Z-score for weight at 36 weeks postconceptional age/discharge ( Δ Z-score

36PCA/DC) were analysed by multivariate linear regression.

Results: 276 infants born 30 to 33 weeks of gestation were studied. Among them, 76 % received parenteral nutrition on central venous line after birth. On day of life 1 (DOL1), 93 % of infants had parenteral amino acids (AA), at an intake ≥ 1.5 g/kg in 27 % of cases. Lipids were started at ≤ DOL2 in 47 % of infants. There was a divergence between the intended and the actual practice for both AA and lipids intake. The AA and energy cumulative deficit (DOL1 to DOL14) were respectively 10.9 ± 8.3 g/kg and 483 ± 181 kcal/kg. Weight Z-score (mean ± SD) significantly decreased from birth ( − 0.17 ± 0.88) to 36 weeks PCA/DC ( − 1.00 ± 0.82) (p < 0.0001), and the extra-uterine growth retardation (EUGR) rate at 36 weeks PCA/DC was 24.2 %. Independent variables associated with Δ Z-score

36PCA/DC were AA cumulative intake and DOL of full enteral feeding.

Conclusions: Nutrition intake was not in compliance with recommendations, and the rate of EUGR was

considerable in this cohort. Efforts are needed to improve adherence to nutrition guidelines and growth outcome of moderately preterm infants.

Keywords: Newborn, Survey, Feeding, Calories, Standards, Growth retard, Parenteral and enteral intake

Background

In the last decades, several studies demonstrated serious cumulative nutritional deficit and extra-uterine growth retardation (EUGR) in preterm infants during the first weeks of life [1–3].

More recently, the causes of this growth failure have been explored and in part identified. The implementation

of continuous education, the carrying out of surveys to focus on trends in clinical practice [4, 5] and the adher- ence of postnatal nutrition to current recommendations, have been addressed as possible solutions for improving growth and reducing EUGR [6, 7].

All this literature relates to extremely or very low birth weight (VLBW) infants and very little is known about the nutritional care of the more “healthy” but still imma- ture babies, born between 30 and 33 weeks of gestational age (GA), even though they account for 15 % of preterm life births and 30 % of neonatal intensive care unit (NICU) admissions.

* Correspondence:silvia.iacobelli@chu-reunion.fr

1Centre d’Etudes Périnatales de l’Océan Indien, CHU La Réunion - Saint Pierre, BP 350 97448 Saint Pierre Cedex, France

2Néonatologie, Réanimation Néonatale et Pédiatrique, CHU La Réunion - Saint Pierre, Saint Pierre Cedex BP 350 97448, France

Full list of author information is available at the end of the article

© 2015 Iacobelli et al.Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Some reports have demonstrated that these infants, too, fail to achieve intrauterine growth rates during hos- pital stay and that significant variations in feeding prac- tices and growth outcomes exist among NICUs [8, 9].

However, to date, no study has evaluated the adherence to guidelines for energy and amino acids (AA) intake in this specific population.

Infants within this cohort are generally less “sick”

when compared with their very preterm counterparts and they have more subtle feeding issues and complica- tions. Moreover, they often require a limited techno- logical support and the choice of avoiding the central venous line (CVL) insertion – in order to reduce the possible associated complications - may limit the supply of the recommended protein and caloric intake, espe- cially during the transitional period [10].

So, the determinants of postnatal growth and the fac- tors influencing the adequacy of nutrition support in moderately preterm babies may be different from those of VLBW infants and deserve a better understanding.

The aims of this study were the following: 1) to de- scribe nutrition practice intentions in a large cohort of moderately premature babies; 2) to compare nutrition practice intentions to actual practice; 3) to describe the adherence of units’ actual practice to current nutrition guidelines; 4) to measure the growth outcomes during hospital stay in this cohort.

Methods

Setting and participants

A survey was carried out in 2014 in French mainland and overseas departments and territories. It was designed to in- clude a heterogeneous group of preterm infants born be- tween 30 and 33 weeks of gestation and cared for in tertiary NICUs or secondary (IIB) level nurseries. For the purpose of this study, infants born between 30 to 33 weeks of gestation were defined “moderately premature babies".

The survey consisted of one-page questionnaire and an electronic file to collect patients’ data. The aims of the questionnaire and of the electronic file were respectively to address the unit nutrition practice intentions and to de- scribe the actual adherence to current nutrition guidelines.

The questionnaire was addressed to the senior phys- ician of each unit or to a delegated colleague having clin- ical experience of neonatal intensive care, and it consisted of multiple choice and open-ended questions.

Specifically for infants born at 30–31 and at 32–33 weeks of gestation, the questionnaire assessed the fol- lowing variables: whether written nutrition guidelines were available in the unit, whether parenteral nutrition (PN) was considered since the day of birth, the type of venous access chosen in case of PN, postnatal day on which parenteral AA and lipid intake was started, AA starting dose, postnatal day on which enteral feeding

was started, enteral feeding advancement and fortifica- tion strategy.

PN was defined as “intravenous nutrition given through a central or peripheral line and containing at least both dextrose and nitrogen”, full enteral feeding as “enteral feed given as sole nutritional source”. Day of life (DOL) 1 was defined as the day of birth.

In each centre, respondents were asked to record data from the last consecutive 12 patients on the electronic file (3 patients for each GA, born from 30 to 33 weeks of gestation) being at 36 weeks postconceptional age (PCA) or discharged from the unit.

Exclusion criteria were: major or digestive congenital anomalies, outborn, transfer to other hospital within DOL14 and death within the first week of life.

Data collection and management

The identity of the respondent to the questionnaire and that of the centre’s electronic file were both blinded for the analysis to all authors. Patients’ records were anonymous.

Data recording for this study was approved by the National Committee for data protection (Commission Nationale de l’Informatique et des Libertés, registra- tion number 1687438).

This study was approved by the institutional medical research ethics committee (Comité de Protection des Personnes Sud-Ouest et Outre Mer III, authorization number 2013/76). According to French legislation, writ- ten parental consent was not needed for this study.

Demographic features and in-hospital morbidities were collected. The following data were recorded on DOL1, 3, 7, 14 and at 36 weeks PCA or at discharge (DC) (when before 36 weeks PCA): weight, parenteral (g/Kg/d of dextrose, AA and lipids) and enteral intake (ml/kg/d of human or given formula milk), whether a central or per- ipheral venous line was inserted.

Mean human milk content was assumed to be 64 kcal⁄dl, 1.4 g/dl of protein, 3.2 g/dl of fat and 7.0 g⁄dl of carbohy- drate. Human milk fortifier and preterm infant formula compositions were based on the product’s labelled nutri- tional content.

Head circumference and length were measured at birth and at 36 weeks PCA/DC. Finally, information was re- trieved on total days of PN on central and peripheral ven- ous line, DOL on which trophic or enteral feeding was started, DOL on which milk fortification was started, type and amount of milk fortifier, DOL of full enteral feeding and maximal postnatal weight loss.

Variables of interest and statistical analysis Nutrition practice intentions

Nutrition practice intentions were compared to the ac- tual practice with regard to the following variables: type of venous access at birth, DOL of initiation of enteral

Iacobelliet al. BMC Pediatrics (2015) 15:110 Page 2 of 7

feeding, DOL of initiation for parenteral AA and lipids and AA starting dose.

Adherence of unit actual practice to current nutrition guidelines

Compliance to nutrition guidelines was measured accord- ing to current European recommendations [11] with the theoretical values recently indicated per GA group [12].

Nutrition intake was considered compliant to guidelines if:

i) AA initiation dose (≥1.5 g/kg/d) was started at DOL1; ii) AA target dose (≥3.5 g/k/d) was attained by DOL7; iii) en- ergy target dose (≥120 kcal/kg/d) was attained by DOL7.

The cumulative AA (g/kg) and energy intake (Kcal/kg) (DOL1 to DOL14) was estimated according to the formula:

Cumulative intake ¼ ð DOL1

1 : 5 Þ þ ð DOL3

3 Þ þ ð DOL7

5 : 5 Þ þ ð DOL14

4 Þ

Formula elaboration and validation

The formula was elaborated based on the assumption that a linear progression of intake occurred between DOL1 to DOL3, DOL3 to DOL7, and DOL7 to DOL14, and it was validated in a subgroup of the cohort study:

in 48 infants (from 4 units) the AA and energy intake was collected daily from DOL1 to DOL14 and the actual cumulative intake (DOL1 to DOL14) was correlated to the cumulative intake estimated by the formula by a lin- ear regression procedure. The model showed a very good regression coefficient (r

= 0.9729; p < 0.001 and 0.9648; p < 0.001 respectively for AA and energy intake).

In all infants, the cumulative deficit (DOL1 to DOL14) for AA and energy was calculated as following:

Cumulative deficit ¼ ðTarget dose14Þ−Cumulative intake

For the purpose of some analyses, infants and centres were split into tertiles of respectively AA cumulative in- take and mean AA cumulative intake.

Growth outcomes

Z-score [mean and standard deviation (SD) for GA] for weight, length and head circumference was calculated at birth and at 36 weeks PCA/DC, according to the refer- ence [13].

Infants were considered SGA when the sex- and age- adjusted weight at birth was below the 10

percentile according to the reference [13].

They were defined EUGR when they were not born SGA and the sex- and age-adjusted weight at birth and at 36 weeks PCA/DC was below the 10

percentile ac- cording to the reference [13].

Simple and multiple linear regressions were performed to investigate variables associated with the delta Z-score for weight at 36 weeks PCA/DC (ΔZ-score

36PCA/DC).

Potential cofounders were selected among antenatal (ste- roids administration, preeclampsia, diabetes, labour, mode of delivery), clinical (GA, gender, singleton birth, SGA, surfactant administration, phototherapy, hypoglycemia, Apgar ≤ 3 at 1 min, neonatal morbidities) and nutritional (CVL insertion at birth, DOL of enteral feeding initiation, DOL of full enteral feeding, tertile of AA cumulative in- take, center tertile for mean AA cumulative intake, cu- mulative energy intake) factors. These were included in the multivariate model only if they were significant at a p value < 0.10. The coefficient of determination (r

) of the model was calculated, in order to choose the best- fit equation for the data set.

Comparisons between groups were performed using χ

-test (or Fisher’s exact test) for categorical variables;

the ANOVA test was used for parametric variables and the Mann–Whitney U test for non-parametric continu- ous variables.

All statistical analyses were carried out using the Med- Calc. ver. 12.3.0.0 statistical software package (MedCalc Software Mariakerke, Belgium) and p values <0.05 were considered statistically significant.

Results

Questionnaire responses and study population

A total of 29 units were surveyed. Four units were sec- ondary excluded as they only provided responses to the questionnaire without feedback of patients’ data.

So, finally, 25 units were included in the analysis (23 III level NICUs and 2 IIB level nurseries).

Data of 276 patients were analysed. Population charac- teristics are presented in Table 1.

Table 2 shows the questionnaires responses (intended practice) according to groups of GA.

Nutritional actual practice

Among the 276 infants, 92 % had a PN and 76 % a CVL for PN. The mean duration of PN on CVL was 9.0 ± 8.1 days.

The average time of initiation of enteral feeding was

1.7 ± 1.2 DOL. Feeding volume (mean ± SD) was ad-

vanced from 9 ± 12 ml/kg/d on DOL1 to 38 ± 26 ml/kg/d

on DOL3, reaching 87 ± 48 ml/kg/d at DOL7 and 140 ±

50 ml/kg/d by DOL14. The average day of full enteral

feeding was 11.7 ± 6.9 DOL. A total of 73 % of all study

subjects received human milk during their hospital stay

and 42 % were at least partially breastfed at 36 weeks

PCA/DC. The average time of initiation of milk fortifier

was 9.9 ± 5.5 DOL. The global rate of milk fortification

was 65 % and 36 % of all infants received fortified feeding

at 36 weeks PCA/DC.

Parenteral AA were started on DOL1 in 93 % of infants, the administered dose at DOL1 was ≥ 1.5 g/kg in 27 % and lipid administration was started at ≤ DOL2 in 47 %. The results on the AA and lipid administration practice and the comparison of the intended and actual practice ac- cording to groups of GA are presented in Table 3.

For the all population study, the AA intake (g/kg/d) was 1.1 ± 0.7 at DOL1; 2.9 ± 0.9 at DOL7, and the energy intake (kcal/kg/d) 94 ± 18 at DOL7. The cumulative AA (g/kg) and energy intake (kcal/kg) were respectively 37.0 ± 8.3 and 1201 ± 166 and the correspondent cumulative deficits were 10.9 ± 8.3 and 483 ± 181.

Growth outcomes

Table 4 details study population Z-scores and ΔZ-scores for anthropometric measures at birth and at 36 weeks PCA/DC.

For the all population study, the maximal postnatal weight loss was 8.3 ± 3.9 %. At 36 weeks PCA/DC the rate of babies whose weight was below the 10

percent- ile according to the reference

was 36.7 % (12.5 % of in- fants being born SGA and 24.2 % having EUGR).

Variables associated with ΔZ-score

36PCA/DC at the univariate analysis were: infant tertile for AA cumulative intake, centre tertile for mean AA cumulative intake, cu- mulative caloric intake, DOL of full enteral feeding, SGA, GA, labour, Apgar ≤ 3 at 1 min of life, photother- apy (data not shown). Variables associated with ΔZ- score at 36 weeks PCA/DC at the multivariate analysis are detailed in Table 5.

Variables associated with cumulative deficit of protein intake (DOL 1–14) at the multivariate analysis are de- tailed in Table 6.

Discussion

This study shows the poor postnatal growth of a moder- ately premature population, demonstrating that both EUGR rate and cumulative nutritional deficit are consid- erable during the first weeks of life in infants born 30 to 33 weeks of gestation. The main result is that a better nutritional intake may significantly reduce the ΔZ- score

from birth to 36 weeks PCA/DC in this vulner- able population.

Critical illness, insufficient early PN support, lack of education and training in PN prescription have been proven responsible for the growth retardation acquired during hospitalization of extremely and VLBW infants [1, 14–16].

To our knowledge, this is the first time that the impact of all these factors on the growth outcome has been ex- plored for the specific population of more healthy but still immature preterm babies. Indeed, several clinical and nu- tritional variables potentially influencing the degree of growth failure have been investigated by this report.

Studies in extremely low birth weight infants have underlined that insufficient early PN support and EUGR are a serious problem, especially for neonates who are small, immature and critically ill, and that they are inde- pendently associated to acute morbidities and illness

Population characteristics (

= 276 preterm infants born

30

33 weeks gestation)

Preeclampsia, n (%) 68 (25.5)

Maternal Diabetes, n (%) 35 (12.8)

Antenatal Steroids, n (%) 251 (91.6)

Singleton Pregnancy, n (%) 62 (22.2)

Infant characteristics

Birth Weight (g), mean ± SD 1582 ± 375

Length (cm), mean ± SD 39.9 ± 3.1

Head Circumference (cm), mean ± SD 28.4 ± 3.9

Gestational Age, n (30/31/32/33) 64/68/76/68

Small for gestational age, n (%) 33 (12)

Male Gender, n (%) 135 (48.9)

Caesarean Section, n (%) 175 (63.6)

Apgar score≤3 at 5 min, n (%) 6 (4.0)

Hypoglycemia requiring treatment, n (%) 36 (13.3)

Phototherapy, n (%) 219 (79.6)

Surfactant Administration, n (%) 85 (30.8)

Mechanical Ventilation, n (%) 91 (33.3)

Early Onset Sepsis, n (%) 12 (4.4)

Late Onset Sepsis, n (%) 29 (10.5)

Necrotizing enterocolitis, n (%) 4 (1.4)

Intraventricular haemorrhage grade 1–2, n (%) 35 (12) Intraventricular haemorrhage grade 3–4, n (%) 2 (0.7) Cystic periventricular leukomalacia, n (%) 5 (1.8)

Hospital Stay (days), mean ± SD 32.5 ± 15.8

Table 2

Questionnaires responses (intended practice) according to groups of GA (25 units)

30-31 weeks 32-33 weeks Written unit guidelines, n (%) 18 (72) 19 (76)

PN started on DOL1, n (%) 22 (88) 14 (56)

CVL for PN, n (%) 11 (44) 4 (16)

AA parenteral initiation, DOL (mean ± SD) 1.08 ± 0.4 1.13 ± 0.6 AA parenteral initiation dose, g (mean ± SD) 1.39 ± 0.59 1.31 ± 0.58 Lipid parenteral initiation, DOL (mean ± SD) 2.0 ± 0.6 2.1 ± 0.4 Enteral Feeding Initiation, DOL (mean ± SD) 1.3 ± 0.5 1.2 ± 0.4 Enteral Feeding Advancement, ml/kg/d

(mean ± SD)

18.2 ± 5.0 19.6 ± 5.6

Mother milk fortification, n (%) 23 (92) 19 (76)

Iacobelliet al. BMC Pediatrics (2015) 15:110 Page 4 of 7

conditions (i.e. need for assisted ventilation, necrotizing enterocolitis) [1].

Recently, Santerre and Rigo [6, 7] have shown that early postnatal nutrition is critical to limit the EUGR and that nutritional policy and growth can be optimized by the respect of current recommendations, even in ba- bies with severe prematurity-related morbidities.

Their observation was assessed in a cohort of ex- tremely and VLBW infants, but based on our results, it may also apply to a more healthy population of larger babies and more advanced GA.

Our study has also documented that shorter time to achieve full enteral feeding was significantly associated with a more favourable growth outcome. This is consist- ent with the results of Ehrenkranz et al. [17], in a pro- spective cohort of VLBW infants and those of Blackwell et al. [8], in a large cohort of healthy, premature infants born between 30 and 35 weeks of gestational age. In this retrospective study, which did not take into account the use of PN, earlier initiation of enteral feeding and higher feeding volumes over the first week of life were corre- lated with lower weight loss during that period.

Interesting also, in our study, cumulative protein def- icit appears significantly lower in babies with lower ges- tational ages and with intrauterine growth retardation, it is inversely associated with centre tertile for mean AA intake and with the use of CVL on DOL1, and it is not influenced by prematurity-related morbidities.

According to all the above data, differences in growth in our population would more clearly reflect differences in nutritional care and may reveal more effective feeding strategies among centres. This result has interesting im- plications for clinicians and NICU policies.

In an original way, this study aimed to evaluate the ad- herence of the intended and the actual practices to the recommended PN guidelines for preterm infants, even if the information was collected within the limits of the starting administration of AA and lipids. It is worthwhile to note that, whether both the practices for DOL of starting AA were in compliance with the established PN guidelines, this was not the case for the AA starting dose, or for lipids administration. This is an important point to be addressed in the course of continuous educa- tion strategies, because, as noticed in a recent report from Fischer and coll. [18], early parenteral lipid intake is positively associated with weight gain in extremely low birth weight infants and may improve early nutri- tional support of preterm neonates.

Finally, our results somehow show a discrepancy be- tween what physicians intend to prescribe and what they do really provide to preterm babies, and this leads to the following considerations: the first one regards the meth- odological limitation of using surveys for the assessment of nutritional protocols, as already highlighted by previ- ous reports [4, 15, 19]; the second one concerns the need of greater efforts to implement the existing known guidelines at the local level in NICUs.

The present study has several limitations. The major one is undoubtedly that our data may not be considered as representative of the entire population of the moderately premature babies targeted by the survey, especially with regards to results of intention- to-treat practices, as questionnaires were not distributed on a national basis, contrary to most surveys [8, 15]. A further point is that some information were not available in our report, that is the rate of daily nutriment

Comparison of the intended and actual practice according to groups of GA (276 infants)

30-31 weeks 32-33 weeks

Intended Practice Actual Practice Intended Practice Actual Practice

CVL for PN (%) 63 92 31 61

Enteral feeding initiation DOL (mean) 1.3 1.9 1.2 1.5

PN started on DOL1 (%) 88 90 56 73

AA parenteral initiation at DOL1 (%) 88 94 88 92

AA parenteral initiation dose≥1.5 g/kg/d (%) 41 33 35 22

Lipid parenteral initiation≤DOL2 (%) 91 54 82 41

Table 4

Z-scores and

Z-scores in 276 preterm infants born 30

33 weeks of gestation

Birth Z-score Z-score 36 weeks PCA/DC ΔZ-score^a p^b

Weight (mean ± SD) −0.17 ± 0.88 −1.00 ± 0.82 −0.80 ± 0.47 <0.0001

Length (mean ± SD) −0.21 ± 1.14 −1.12 ± 1.09 −0.90 ± 0.91 <0.0001

Head Circumference (mean ± SD) 0.04 ± 1.04 −0.41 ± 0.92 −0.41 ± 0.74 <0.0001

aΔZ-score from birth to 36 weeks PCA/DC.^bZ-score 36 weeks PCA/DC versus Birth Z-score (ANOVA for repeated measures)

progression, the unit contraindications to enteral and parenteral feeding advancement, the presence of meta- bolic abnormalities (acidosis, hyperglycemia, hypertriglyc- eridemia) during the first days of life, the incidence of sepsis associated to CVL and finally the type of solutions, additive and supplements used in PN. The model of mul- tiple linear regression used to identify factors associated with ΔZ-score

at 36 weeks PCA/DC has a quite poor general coefficient, suggesting that other variables not considered in the analysis may account for explaining the growth outcome in the studied population. Finally, the present investigation was not designed to explore enteral feeding practices in detail in terms of fortification strat- egies, feeding techniques and breastfeeding polices, which might produce differences in growth outcome, as illus- trated by other studies [20, 21].

Conclusions

The results of our report have interesting implications for clinicians and NICU policymakers. As already dem- onstrated for extremely and VLBW infants, our study al- lows to conclude that the nutrition delivered to infants born 30–33 weeks gestation is often not in compliance with international guidelines, and that this is associated with considerable rates of EUGR.

The reasons for suboptimal AA and total calories de- livery in this specific population mainly reside on unit nutrition practice and feeding strategies, this making that the growth outcome may be improved.

Factors influencing EUGR in moderately premature babies are not fully elucidated, and further studies are needed to identify practices associated with better growth in this quite healthy, but still vulnerable infant population.

Abbreviations

AA:Amino acids; CVL: Central venous line; DC: Discharge; DOL: Day of life;

ΔZ-score_w36PCA/DC:ΔZ-score for weight at 36 weeks postconceptional age/discharge; EUGR: Extra-uterine growth retardation; GA: Gestational age;

NICU: Neonatal intensive care unit; SD: Standard deviation; SGA: Small for gestational age; VLBW: Very low birth weight; PCA: Postconceptional age.

Competing interests

The authors wish to confirm that there are no conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

Authors’contributions

SI conceptualized and designed the study, carried out the interpretation of the data and wrote the paper. MV participated to the study design, performed the acquisition of the data and participated to the interpretation of the data. AL participated to the study design and critically revised the manuscript. PYR participated to the acquisition and analysis of the data. JBG critically reviewed and revised the manuscript drafts. FB participated to the draft of the initial manuscript, performed the statistical analysis, provided to a substantial contribution to data interpretation and revised the manuscript drafts. All the authors read and approved the final manuscript as submitted.

Acknowledgements

With thanks to Madame Isabelle Germain, executive secretary at Centre d’Études Périnatales de l’Océan Indien (CHU La Réunion) who played a crucial role in this study. All the medical doctors collaborating on the NUTRIQUAL French group: Tasmine Akbaraly, CH Perpignan; Dominique Astruc, CHU Strasbourg; Brigitte Auburtin, CH Epinal; Isabelle Bauvin, CH Pau;

Antoine Bedu, CHU Limoges; Faouzi Benababdelmalek, CH Nevers; Amandine Blasquez, CH Libourne; Farid Boubred, AP-HP Marseille; Henri Bruel, CH Le Havre; Gilles Cambonie, CHRU Montpellier; Magali Carbonnier, CHU La Réunion (Saint-Pierre); Daniele De Luca, Antoine Béclère - GH Paris Sud;

Celine Dillenseger, CHU Strasbourg; Benoît Dumont,CHU Saint Etienne;

Michel Françoise, CH Chalon sur Saône; Julie Guerreiro, CHR Orléans; Joel Hodonou CH Périgueux; Khaled Husseini, CHU Poitiers; Pierre-Henry Jarraud, Port-Royal - Hôpital Cochin AP-PH Paris; Philippe Jouvencel, CHIC Bayonne;

Serge Klosowski, CH Lens; Laura Kollen, CH Perpignan; Davi Komlan, CH Cayenne; Aurélie Labaste, CH Chalon sur Saône; Doriane Madelenau, Port-Royal - Hôpital Cochin AP-PH Paris; Florence Masson, CHRU Montpellier;

Anne-Claude Menguy, CH Perpignan; Myriam Mirc, CHI André-Gregoire, Montreuil; Fadilha Mokraoui, Antoine Béclère - GH Paris Sud; Julien Moursie, CH Le Havre; Jean-René Nelson, CH Libourne; Laurence Pognon, CHRU Lille;

Duksha Ramful, CHU La Réunion (Saint Denis); Olivier Romain, Antoine Béclère - GH Paris Sud; Sylvaine Rousseau, CH Roubaix; Denis Semama, CHU Dijon; Laurent Storme, CHRU Lille; Amélie Vintéjoux, CH Macon; Carlos Varela, CHU Guadeloupe. The collaborators have no conflict of interest, funding sources, and industry-relation to report.

Author details

1Centre d’Etudes Périnatales de l’Océan Indien, CHU La Réunion - Saint Pierre, BP 350 97448 Saint Pierre Cedex, France.²Néonatologie, Réanimation Néonatale et Pédiatrique, CHU La Réunion - Saint Pierre, Saint Pierre Cedex BP 350 97448, France.³Department of Neonatology, APHP Necker Enfants Malades Hospital, Paris, France.⁴Paris Descartes University, Paris, France.

Received: 7 April 2015 Accepted: 20 August 2015

References

1. Clark RH, Thomas P, Peabody J. Extrauterine growth restriction remains a serious problem in prematurely born neonates. Pediatrics. 2003;111(5 Pt 1):986–90.

Table 5

Variables associated with

Z-score

at 36 weeks PCA/DC in 276 preterm infants born 30

33 weeks of gestation. Multiple linear regression, general coefficient of the model

= 0.10,

< 0.001

Variables Coefficient r^partial p

Tertile for AA cumulative intake 0.13 0.22 <0.001 DOL of full enteral feeding −0.01 −0.18 0.005

Small for Gestational Age 0.16 0.12 0.06

Gestational Age 0.05 0.12 0.07

Table 6

Variables associated with cumulative deficit of protein intake (DOL 1

14) at the multivariate analysis in 276 preterm infants born 30

33 weeks of gestation

Variables Coefficient r^partial p

Center tertile for mean AA intake −4.3 0.50 <0.001

PN in CVL at day1 −3.8 0.27 <0.001

DOL of full enteral feeding −0.23 0.23 <0.001

Gestational Age 1.3 −0.22 <0.001

Small for Gestational Age −2.8 0.14 0.01

Preeclampsia −1.8 0.13 0.03

Iacobelliet al. BMC Pediatrics (2015) 15:110 Page 6 of 7

2. Embleton NE, Pang N, Cooke RJ. Postnatal malnutrition and growth retardation: an inevitable consequence of current recommendations in preterm infants? Pediatrics. 2001;107:270–3.

3. Olsen IE, Richardson DK, Schmid CH, Ausman LM, Dwyer JT. Intersite differences in weight growth velocity of extremely premature infants.

Pediatrics. 2002;110:1125–32.

4. Lapillonne A, Kermorvant-Duchemin E. A systematic review of practice surveys on parenteral nutrition for preterm infants. J Nutr. 2013;143 Suppl 12:2061–5.

5. Hans DH, Pylipow M, Long JD, Thureen PJ, Georgieff MK. Nutritional Practices in the Neonatal Intensive Care Unit: Analysis of a 2006 Neonatal Nutrition Survey. Pediatrics. 2009;123:51–8.

6. Senterre T, Rigo J. Optimizing early nutritional support based on recent recommendations in VLBW infants allows abolishing postnatal growth restriction. J Pediatr Gastroenterol Nutr. 2011;53(5):536–42.

7. Senterre T, Rigo J. Reduction in postnatal cumulative nutritional deficit and improvement of growth in extremely preterm infants. Acta Paediatr.

2012;101(2):e64–70.

8. Blackwell M, Eichenwald E, McAlmon K, Petit K, Thomson Linton P, McCormick MC, et al. Interneonatal intensive care unit variation in growth rates and feeding practice in healthy moderately premature infants. J Perinatol. 2005;25:478–85.

9. Lee JS, Richardson DK, Clark RH. Postnatal growth of infants 30–34 weeks gestational age: A comparison of 63 neonatal intensive care units (NICUs).

Pediatr Res. 2001;49 Suppl 2:358A.

10. Gouyon JB, Iacobelli S, Ferdynus C, Bonsante F. Neonatal problems of late and moderate preterm infants. Semin Fetal Neonatal Med. 2012;17(3):146–52.

11. Koletzko B, Goulet O, Hunt J, Krohn K, Shamir R. Guidelines on Paediatric Parenteral Nutrition of the European Society of Pediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) and the European Society for Clinical Nutrition and Metabolism (ESPEN), supported by the European Society of Paediatric Research (ESPR). J Pediatr Gastroenterol Nutr. 2005;41 Suppl 2:1–87.

12. Lapillonne A, O'Connor DL, Wang D, Rigo J. Nutritional recommendations for the late-preterm infant and the preterm infant after hospital discharge. J Pediatr. 2013;162 Suppl 3:90–100.

13. Fenton 2013 Growth Calculator for Preterm Infants. Available from http://

www.peditools.org/fenton2013. Accessed 20 Jan 2015.

14. Grover A, Khashu M, Mukherjee A, Kairamkonda V. Iatrogenic malnutrition in neonatal intensive care units: urgent need to modify practice. J Parenter Enteral Nutr. 2008;32:140–4.

15. Lapillonne A, Fellous L, Mokthari M, Kermorvant-Duchemin E. Parenteral nutrition objectives for very low birth weight infants: results of a national survey. J Pediatr Gastroenterol Nutr. 2009;48:618–26.

16. Ahmed M, Irwin S, Tuthill DP. Education and evidence are needed to improve neonatal parenteral nutrition practice. J Parenter Enteral Nutr. 2004;28:176–9.

17. Ehrenkranz RA, Younes N, Lemons JA, Fanaroff AA, Donovan EF, Wright LL, et al. Longitudinal growth of hospitalized very low birth weight infants.

Pediatrics. 1999;104(2 Pt 1):280–9.

18. Fischer CJ, Maucort-Boulch D, Essomo Megnier-Mbo CM, Remontet L, Claris O. Early parenteral lipids and growth velocity in extremely-low-birth-weight infants. Clin Nutr. 2014;33:502–8.

19. Lapillonne A, Carnielli VP, Embleton ND, Mihatsch W. Quality of newborn care: adherence to guidelines for parenteral nutrition in preterm infants in four European countries.BMJ Open.2013; doi:10.1136/bmjopen-2013-003478.

20. Hair AB, Blanco CL, Moreira AG, Hawthorne KM, Lee ML, Rechtman DJ, et al.

Randomized trial of human milk cream as a supplement to standard fortification of an exclusive human milk-based diet in infants 750–1250 g birth weight. J Pediatr. 2014;165(5):915–20.

21. Zecca E, Costa S, Barone G, Giordano L, Zecca C, Maggio L. Proactive enteral nutrition in moderately preterm small for gestational age infants: a randomized clinical trial. J Pediatr. 2014;165(6):1135–9.

Submit your next manuscript to BioMed Central and take full advantage of:

• Convenient online submission

• Thorough peer review

• No space constraints or color figure charges

• Immediate publication on acceptance

• Inclusion in PubMed, CAS, Scopus and Google Scholar

• Research which is freely available for redistribution

Submit your manuscript at www.biomedcentral.com/submit